Modeling and Analyzing Xylem Vulnerability to Embolism as an Epidemic Process.

Xylem vulnerability to embolism can be quantified by "vulnerability curves" (VC) that are obtained by subjecting wood samples to increasingly negative water potential and monitoring the progressive loss of hydraulic conductivity. VC are typically sigmoidal, and various approaches are used to fit the experimentally obtained VC data for extracting benchmark data of vulnerability to embolism. In addition to such empirical methods, mechanistic approaches to calculate embolism propagation are epidemic modeling and network theory. Both describe the transmission of "objects" (in this case, the transmission of gas) between interconnected elements. In network theory, a population of interconnected elements is described by graphs in which objects are represented by vertices or nodes and connections between these objections as edges linking the vertices. A graph showing a population of interconnected xylem conduits represents an "individual" wood sample that allows spatial tracking of embolism propagation. In contrast, in epidemic modeling, the transmission dynamics for a population that is subdivided into infection-relevant groups is calculated by an equation system. For this, embolized conduits are considered to be "infected," and the "infection" is the transmission of gas from embolized conduits to their still water-filled neighbors. Both approaches allow for a mechanistic simulation of embolism propagation.

Toward a Cenozoic history of atmospheric CO2.

The geological record encodes the relationship between climate and atmospheric carbon dioxide (CO2) over long and short timescales, as well as potential drivers of evolutionary transitions. However, reconstructing CO2 beyond direct measurements requires the use of paleoproxies and herein lies the challenge, as proxies differ in their assumptions, degree of understanding, and even reconstructed values. In this study, we critically evaluated, categorized, and integrated available proxies to create a high-fidelity and transparently constructed atmospheric CO2 record spanning the past 66 million years. This newly constructed record provides clearer evidence for higher Earth system sensitivity in the past and for the role of CO2 thresholds in biological and cryosphere evolution.

Ambient aerosols increase stomatal transpiration and conductance of hydroponic sunflowers by extending the hydraulic system to the leaf surface.

Introduction: Many atmospheric aerosols are hygroscopic and play an important role in cloud formation. Similarly, aerosols become sites of micro-condensation when they deposit to the upper and lower surfaces of leaves. Deposited salts, in particular can trigger condensation at humidities considerably below atmospheric saturation, according to their hygroscopicity and the relative humidity within the leaf boundary layer. Salt induced water potential gradients and the resulting dynamics of concentrated salt solutions can be expected to affect plant water relations. Methods: Hydroponic sunflowers were grown in filtered (FA) and unfiltered, ambient air (AA). Sap flow was measured for 18 days and several indicators of incipient drought stress were studied. Results: At 2% difference in mean vapor pressure deficit (D), AA sunflowers had 49% higher mean transpiration rates, lower osmotic potential, higher proline concentrations, and different tracer transport patterns in the leaf compared to FA sunflowers. Aerosols increased plant conductance particularly at low D. Discussion: The proposed mechanism is that thin aqueous films of salt solutions from deliquescent deposited aerosols enter into stomata and cause an extension of the hydraulic system. This hydraulic connection leads - parallel to stomatal water vapor transpiration - to wick-like stomatal loss of liquid water and to a higher impact of D on plant water loss. Due to ample water supply by hydroponic cultivation, AA plants thrived as well as FA plants, but under more challenging conditions, aerosol deposits may make plants more susceptible to drought stress.

The Plant Leaf: A Biomimetic Resource for Multifunctional and Economic Design.

As organs of photosynthesis, leaves are of vital importance for plants and a source of inspiration for biomimetic developments. Leaves are composed of interconnected functional elements that evolved in concert under high selective pressure, directed toward strategies for improving productivity with limited resources. In this paper, selected basic components of the leaf are described together with biomimetic examples derived from them. The epidermis (the "skin" of leaves) protects the leaf from uncontrolled desiccation and carries functional surface structures such as wax crystals and hairs. The epidermis is pierced by micropore apparatuses, stomata, which allow for regulated gas exchange. Photosynthesis takes place in the internal leaf tissue, while the venation system supplies the leaf with water and nutrients and exports the products of photosynthesis. Identifying the selective forces as well as functional limitations of the single components requires understanding the leaf as an integrated system that was shaped by evolution to maximize carbon gain from limited resource availability. These economic aspects of leaf function manifest themselves as trade-off solutions. Biomimetics is expected to benefit from a more holistic perspective on adaptive strategies and functional contexts of leaf structures.

An integrated leaf trait analysis of two Paleogene leaf floras.

Objectives: This study presents the Integrated Leaf Trait Analysis (ILTA), a workflow for the combined application of methodologies in leaf trait and insect herbivory analyses on fossil dicot leaf assemblages. The objectives were (1) to record the leaf morphological variability, (2) to describe the herbivory pattern on fossil leaves, (3) to explore relations between leaf morphological trait combination types (TCTs), quantitative leaf traits, and other plant characteristics (e.g., phenology), and (4) to explore relations of leaf traits and insect herbivory. Material and Methods: The leaves of the early Oligocene floras Seifhennersdorf (Saxony, Germany) and Suletice-Berand (Ústí nad Labem Region, Czech Republic) were analyzed. The TCT approach was used to record the leaf morphological patterns. Metrics based on damage types on leaves were used to describe the kind and extent of insect herbivory. The leaf assemblages were characterized quantitatively (e.g., leaf area and leaf mass per area (LMA)) based on subsamples of 400 leaves per site. Multivariate analyses were performed to explore trait variations. Results: In Seifhennersdorf, toothed leaves of TCT F from deciduous fossil-species are most frequent. The flora of Suletice-Berand is dominated by evergreen fossil-species, which is reflected by the occurrence of toothed and untoothed leaves with closed secondary venation types (TCTs A or E). Significant differences are observed for mean leaf area and LMA, with larger leaves tending to lower LMA in Seifhennersdorf and smaller leaves tending to higher LMA in Suletice-Berand. The frequency and richness of damage types are significantly higher in Suletice-Berand than in Seifhennersdorf. In Seifhennersdorf, the evidence of damage types is highest on deciduous fossil-species, whereas it is highest on evergreen fossil-species in Suletice-Berand. Overall, insect herbivory tends to be more frequently to occur on toothed leaves (TCTs E, F, and P) that are of low LMA. The frequency, richness, and occurrence of damage types vary among fossil-species with similar phenology and TCT. In general, they are highest on leaves of abundant fossil-species. Discussion: TCTs reflect the diversity and abundance of leaf architectural types of fossil floras. Differences in TCT proportions and quantitative leaf traits may be consistent with local variations in the proportion of broad-leaved deciduous and evergreen elements in the ecotonal vegetation of the early Oligocene. A correlation between leaf size, LMA, and fossil-species indicates that trait variations are partly dependent on the taxonomic composition. Leaf morphology or TCTs itself cannot explain the difference in insect herbivory on leaves. It is a more complex relationship where leaf morphology, LMA, phenology, and taxonomic affiliation are crucial.

Foliar water uptake in Pinus species depends on needle age and stomatal wax structures.

BACKGROUND AND AIMS: Foliar water uptake (FWU) has been documented in many species and is increasingly recognized as a non-trivial factor in plant-water relationships. However, it remains unknown whether FWU is a widespread phenomenon in Pinus species, and how it may relate to needle traits such as the form and structure of stomatal wax plugs. In this contribution, these questions were addressed by studying FWU in current-year and 1-year-old needles of seven Pinus species. METHODS: We monitored FWU gravimetrically and analysed the needle surface via cryo-scanning electron microscopy. Additionally, we considered the effect of artificial wax erosion by application of the surfactant Triton X-100, which is able to alter wax crystals. KEY RESULTS: The results show for all species that (1) FWU occurred, (2) FWU is higher in old needles compared to young needles and (3) there is substantial erosion of stomatal wax plugs in old needles. FWU was highest in Pinus canariensis, which has a thin stomatal wax plug. Surfactant treatment enhanced FWU. CONCLUSIONS: The results of this study provide evidence for (1) widespread FWU in Pinus, (2) the influence of stomatal wax plugs on FWU and (3) age-related needle surface erosion.

Straight roads into nowhere - obvious and not-so-obvious biological models for ferrophobic surfaces.

There are currently efforts to improve strategies for biomimetic approaches, to identify pitfalls and to provide recommendations for a successful biomimetic work flow. In this contribution, a case study of a concrete biomimetic project is described that started with a posed technical problem for which seemingly obvious biological models exist. The technical problem was to devise a ferrophobic surface that prevents the contact between the copper surface of a tuyère (a water cooled aeration pipe within a blast furnace) and liquid iron. Therefore, biological external surfaces that strongly repel liquids appeared to be suitable, particularly the hair cover of the water fern Salvinia molesta and the surface of Collembola (an arthropod group). It turned out, however, that it was not feasible to realise the functional structures of both biological models for the tuyère problem. Instead, a seemingly not obvious biological model was identified, namely micropores within the cell walls of water-transporting conduits of plants that connect the conduits to a three-dimensional flow network. These specially shaped pores are assumed to be able to create stable air bodies, which support the refilling of embolised conduits. By adopting the shape of these micropores, a successful prototype for a ferrophobic copper surface repelling liquid iron could be devised. This case study illustrates that straight road maps from technical problems to obvious biological models are no guarantee for success, and that it is difficult to arrive at a formalised biomimetic working scheme. Rather, a broad understanding of biological function and its complexity is beneficial.

How much biology is in the product? Role and relevance of biological evolution and function for bio-inspired design.

Bio-inspired design (BID) means the concept of transferring functional principles from biology to technology. The core idea driving BID-related work is that evolution has shaped functional attributes, which are termed "adaptations" in biology, to a high functional performance by relentless selective pressure. For current methods and tools, such as data bases, it is implicitly supposed that the considered biological models are adaptations and their functions already clarified. Often, however, the identification of adaptations and their functional features is a difficult task which is not yet accomplished for numerous biological structures, as happens to be the case also for various organismic features from which successful BID developments were derived. This appears to question the relevance of the much stressed importance of evolution for BID. While it is obviously possible to derive an attractive technical principle from an observed biological effect without knowing its original functionality, this kind of BID ("analog BID") has no further ties to biology. In contrast, a BID based on an adaptation and its function ("homolog BID") is deeply embedded in biology. It is suggested that a serious and honest clarification of the functional background of a biological structure is an essential first step in devising a BID project, to recognize possible problems and pitfalls as well as to evaluate the need for further biological analysis.

When rain collides with plants-patterns and forces of drop impact and how leaves respond to them.

Raindrop impact on leaves is a common event which is of relevance for numerous processes, including the dispersal of pathogens and propagules, leaf wax erosion, gas exchange, leaf water absorption, and interception and storage of rainwater by canopies. The process of drop impact is complex, and its outcome depends on many influential factors. The wettability of plants has been recognized as an important parameter which is itself complex and difficult to determine for leaf surfaces. Other important parameters include leaf inclination angle and the ability of leaves to respond elastically to drop impact. Different elastic motions are initiated by drop impact, including local deformation, flapping, torsion, and bending, as well as 'swinging' of the petiole. These elastic responses, which occur on different time scales, can affect drop impact directly or indirectly, by changing the leaf inclination. An important feature of drop impact is splashing, meaning the fragmentation of the drop with ejection of satellite droplets. This process is promoted by the kinetic energy of the drop and leaf traits. For instance, a dense trichome cover can suppress splashing. Basic drop impact patterns are presented and discussed for a number of different leaf types, as well as some exemplary mosses.

The impact of raindrops on Salvinia molesta leaves: effects of trichomes and elasticity.

The floating leaves of the aquatic fern Salvinia molesta are covered by superhydrophobic hairs (=trichomes) which are shaped like egg-beaters. These trichomes cause high water repellency and stable unwettability if the leaf is immersed. Whereas S. molesta hairs are technically interesting, there remains also the question concerning their biological relevance. S. molesta has its origin in Brazil within a region exposed to intense rainfall which easily penetrates the trichome cover. In this study, drop impact on leaves of S. molesta were analysed using a high-speed camera. The largest portion of the kinetic energy of a rain drop is absorbed by elastic responses of the trichomes and the leaf. Although rain water is mostly repelled, it turned out that the trichomes hamper swift shedding of rain water and some residual water can remain below the 'egg-beaters'. Drops rolling over the trichomes can, however, 'suck up' water trapped beneath the egg-beaters because the energetic state of a drop on top of the trichomes is-on account of the superhydrophobicity of the hairs-much more favourable. The trichomes may therefore be beneficial during intense rainfall, because they absorb some kinetic energy and keep the leaf base mostly free from water.

A model for extracellular freezing based on observations on Equisetum hyemale.

In frost hardy plants, the lethal intracellular formation of ice crystals has to be prevented during frost periods. Besides the ability for supercooling and pre-frost dehydration of tissues, extracellular ice formation is another strategy to control ice development in tissues. During extracellular ice formation, partially large ice bodies accumulate in intercellular spaces, often at preferred sites which can also be expandable. In this contribution, the physico-chemical processes underlying the water movements towards the sites of extracellular ice formation are studied theoretically, based on observations on the frost hardy horsetail species Equisetum hyemale, with the overall aim to obtain a better understanding of the physical processes involved in extracellular ice formation. In E. hyemale, ice accumulates in the extensive internal canal system. The study focuses on the processes which are triggered in the cellular osmotic-mechanic system by falling, and especially subzero temperatures. It can be shown that when the temperature falls, (1) water flow out of cells is actuated and (2) "stiff-walled" cells lose less water than "soft-walled" cells. Furthermore, (3) cell water loss increases with increasing (= less negative) turgor loss point. These processes are not related to any specific activities of the cell but are solely a consequence of the structure of the cellular osmotic system. On this basis, a directed water flow can be initiated triggered by subzero temperatures. The suggested mechanism may be quite common in frost hardy species with extracellular ice formation.

Xylem functioning, dysfunction and repair: a physical perspective and implications for phloem transport.

Xylem and phloem are the two main conveyance systems in plants allowing exchanges of water and carbohydrates between roots and leaves. While each system has been studied in isolation for well over a century, the coupling and coordination between them remains the subject of inquiry and active research and frames the scope of the review here. Using a set of balance equations, hazards of bubble formation and their role in shaping xylem pressure and its corollary impact on phloem pressure and sugar transport are featured. The behavior of an isolated and freely floating air bubble within the xylem is first analyzed so as to introduce key principles such as the Helmholtz free energy and its links to embryonic bubble sizes. These principles are extended by considering bubbles filled with water vapor and air arising from air seeding. Using this framework, key results about stability and hazards of bubbles in contact with xylem walls are discussed. A chemical equilibrium between phloem and xylem systems is then introduced to link xylem and osmotic pressures. The consequences of such a link for sugar concentration needed to sustain efficient phloem transport by osmosis in the loading zone is presented. Catastrophic cases where phloem dysfunction occurs are analyzed in terms of xylem function and its vulnerability to cavitation. A link between operating pressures in the soil system bounded by field capacity and wilting points and maintenance of phloem functioning are discussed as conjectures to be tested in the future.

Computational Fluid Dynamics Analysis of the Fossil Crinoid Encrinus liliiformis (Echinodermata: Crinoidea).

Crinoids, members of the phylum Echinodermata, are passive suspension feeders and catch plankton without producing an active feeding current. Today, the stalked forms are known only from deep water habitats, where flow conditions are rather constant and feeding velocities relatively low. For feeding, they form a characteristic parabolic filtration fan with their arms recurved backwards into the current. The fossil record, in contrast, provides a large number of stalked crinoids that lived in shallow water settings, with more rapidly changing flow velocities and directions compared to the deep sea habitat of extant crinoids. In addition, some of the fossil representatives were possibly not as flexible as today's crinoids and for those forms alternative feeding positions were assumed. One of these fossil crinoids is Encrinus liliiformis, which lived during the middle Triassic Muschelkalk in Central Europe. The presented project investigates different feeding postures using Computational Fluid Dynamics to analyze flow patterns forming around the crown of E. liliiformis, including experimental validation by Particle Image Velocimetry. The study comprises the analysis of different flow directions, velocities, as well as crown orientations. Results show that inflow from lateral and oral leads to direct transport of plankton particles into the crown and onto the oral surface. With current coming from the "rear" (aboral) side of the crinoid, the conical opening of the crown produces a backward oriented flow in its wake that transports particles into the crown. The results suggest that a conical feeding position may have been less dependent on stable flow conditions compared to the parabolic filtration fan. It is thus assumed that the conical feeding posture of E. liliiformis was suitable for feeding under dynamically changing flow conditions typical for the shallow marine setting of the Upper Muschelkalk.

Diurnal pattern of stomatal conductance in the large-leaved temperate liana Aristolochia macrophylla depends on spatial position within the leaf lamina.

BACKGROUND AND AIMS: The large distance between peripheral leaf regions and the petiole in large leaves is expected to cause stronger negative water potentials at the leaf apex and marginal zones compared with more central or basal leaf regions. Leaf zone-specific differences in water supply and/or gas exchange may therefore be anticipated. In this study, an investigation was made to see whether zonal differences in gas exchange regulation can be detected in large leaves. METHODS: The diurnal course of stomatal conductance, gs, was monitored at defined lamina zones during two consecutive vegetation periods in the liana Aristolochia macrophylla that has large leaves. Local climate and stem water potential were also monitored to include parameters involved in stomatal response. Additionally, leaf zonal vein densities were measured to assess possible trends in local hydraulic supply. KEY RESULTS: It was found that the diurnal pattern of gs depends on the position within a leaf in A. macrophylla. The highest values during the early morning were shown by the apical region, with subsequent decline later in the morning and a further gradual decline towards the evening. The diurnal pattern of gs at the marginal regions was similar to that of the leaf tip but showed a time lag of about 1 h. At the leaf base, the diurnal pattern of gs was similar to that of the margins but with lower maximum gs. At the the leaf centre regions, gs tended to show quite constant moderate values during most of the day. Densities of minor veins were lower at the margin and tip compared with the centre and base. CONCLUSIONS: Gas exchange regulation appears to be zone specific in A. macrophylla leaves. It is suggested that the spatial-diurnal pattern of gs expressed by A. macrophylla leaves represents a strategy to prevent leaf zonal water stress and subsequent vein embolism.

Visualization of embolism formation in the xylem of liana stems using neutron radiography.

BACKGROUND AND AIMS: Cold neutron radiography was applied to directly observe embolism in conduits of liana stems with the aim to evaluate the suitability of this method for studying embolism formation and repair. Potential advantages of this method are a principally non-invasive imaging approach with low energy dose compared with synchrotron X-ray radiation, a good spatial and temporal resolution, and the possibility to observe the entire volume of stem portions with a length of several centimetres at one time. METHODS: Complete and cut stems of Adenia lobata, Aristolochia macrophylla and Parthenocissus tricuspidata were radiographed at the neutron imaging facility CONRAD at the Helmholtz-Zentrum Berlin für Materialien und Energie, with each measurement cycle lasting several hours. Low attenuation gas spaces were separated from the high attenuation (water-containing) plant tissue using image processing. KEY RESULTS: Severe cuts into the stem were necessary to induce embolism. The formation and temporal course of an embolism event could then be successfully observed in individual conduits. It was found that complete emptying of a vessel with a diameter of 100 µm required a time interval of 4 min. Furthermore, dehydration of the whole stem section could be monitored via decreasing attenuation of the neutrons. CONCLUSIONS: The results suggest that cold neutron radiography represents a useful tool for studying water relations in plant stems that has the potential to complement other non-invasive methods.

Stomatal encryption by epicuticular waxes as a plastic trait modifying gas exchange in a Mediterranean evergreen species (Quercus coccifera L.).

The adaptive benefit of stomatal crypts remains a matter of controversy. This work studies the effect on gas exchange of cuticular rims that overarch the stomatal pore in the Mediterranean species Quercus coccifera L. growing under Mediterranean (lower relative humidities and high summer temperatures) or oceanic conditions (higher daily relative humidities and mild temperatures). After microscopic assessment of the leaf surfaces and stomatal architecture, the impact of the cuticular 'cup' on gas exchange was evaluated by employing three-dimensional finite element models. Here, we provide evidence for a high plasticity of the Q. coccifera cuticular cup, with much larger vents under oceanic conditions compared to small vents under Mediterranean conditions. This structure adds a substantial fixed resistance thereby strongly decreasing gas exchange under Mediterranean conditions. The cuticular cup, which also increases leaf internal humidity, might buffer the rapid changes in vapour pressure deficit (VPD) often observed under Mediterranean conditions. Since water loss of guard and adjacent epidermal cells regulates stomatal aperture, we suggest that this structure allows an efficient regulation of stomatal conductance and optimum use of resources under high VPD. This study provides evidence that plasticity of stomatal architecture can be an important structural component of hydraulic adaptation to different climate conditions.

Sorting of droplets by migration on structured surfaces.

BACKGROUND: Controlled transport of microdroplets is a topic of interest for various applications. It is well known that liquid droplets move towards areas of minimum contact angle if placed on a flat solid surface exhibiting a gradient of contact angle. This effect can be utilised for droplet manipulation. In this contribution we describe how controlled droplet movement can be achieved by a surface pattern consisting of cones and funnels whose length scales are comparable to the droplet diameter. RESULTS: The surface energy of a droplet attached to a cone in a symmetry-preserving way can be smaller than the surface energy of a freely floating droplet. If the value of the contact angle is fixed and lies within a certain interval, then droplets sitting initially on a cone can gain energy by moving to adjacent cones. CONCLUSION: Surfaces covered with cone-shaped protrusions or cavities may be devised for constructing "band-conveyors" for droplets. In our approach, it is essentially the surface structure which is varied, not the contact angle. It may be speculated that suitably patterned surfaces are also utilised in biological surfaces where a large variety of ornamentations and surface structuring are often observed.

Stomatal crypts have small effects on transpiration: a numerical model analysis.

Stomata arranged in crypts with trichomes are commonly considered to be adaptations to aridity due to the additional diffusion resistance associated with this arrangement; however, information on the effect of crypts on gas exchange, relative to stomata, is sparse. In this study, three-dimensional Finite Element models of encrypted stomata were generated using commercial Computational Fluid Dynamics software. The models were based on crypt and stomatal architectural characteristics of the species Banksia ilicifolia, examined microscopically, and variations thereof. In leaves with open or partially closed stomata, crypts reduced transpiration by less than 15% compared with nonencrypted, superficially positioned stomata. A larger effect of crypts was found only in models with unrealistically high stomatal conductances. Trichomes inside the crypt had virtually no influence on transpiration. Crypt conductance varied with stomatal conductance, boundary layer conductance, and ambient relative humidity, as these factors modified the three-dimensional diffusion patterns inside crypts. It was concluded that it is unlikely that the primary function of crypts and crypt trichomes is to reduce transpiration.

Computer-based studies of diffusion through stomata of different architecture.

BACKGROUND AND AIMS: The influence of stomatal architecture on stomatal conductance and on the developing concentration gradient was explored quantitatively by comparing diffusion rates of water vapour and CO(2) occurring in a set of three-dimensional stoma models. The influence on diffusion of an internal cuticle, a sunken stoma, a partially closed stoma and of substomatal chambers of two different sizes was considered. METHODS: The study was performed by using a commercial computer program based on the Finite Element Method which allows for the simulation of diffusion in three dimensions. By using this method, diffusion was generated by prescribed gas concentrations at the boundaries of the substomatal chamber and outside of the leaf. The program calculates the distribution of gas concentrations over the entire model space. KEY RESULTS: Locating the stomatal pore at the bottom of a stomatal antechamber with a depth of 20 microm decreased the conductance significantly (at roughly about 30 %). The humidity directly above the stomatal pore is significantly higher with the stomatal antechamber present. Lining the walls of the substomatal chamber with an internal cuticle which suppresses evaporation had an even stronger effect by reducing the conductance to 60 % of the original value. The study corroborates therefore the results of former studies that water will evaporate preferentially at sites in the immediate vicinity to the stomatal pore if no internal cuticle is present. The conductance decrease affects only water vapour and not CO(2). Increasing the substomatal chamber increases CO(2) uptake, whereas transpiration increases if an internal cuticle is present. CONCLUSIONS: Variation of stomatal structure may, with unchanged pore size and depth, profoundly affect gas exchange and the pathways of liquid water inside the leaf. Equations for calculation of stomatal conductance which are solely based on stomatal density and pore depth and size can significantly overestimate stomatal conductance.